Tansley reviewThe evolution of the land plant lifecycleAuthor for correspondence:Karl J. NiklasTel: 001 607 255 8727Email: kjn2@cornell.eduReceived: 20 July 2009Accepted: 1 September 2009Karl J. Niklas1and Ulrich Kutschera21Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA;2Institute of Biology,University of Kassel, Heinrich-Plett-Strasse 40, D-34109 Kassel, GermanyNew Phytologist (2010) 185: 2741doi: 10.1111/j.1469-8137.2009.03054.xKey words: alternation of generations,archegonia, Chara, Cooksonia,homeodomain gene networks, homology,life cycle evolution, MADS-box genes.SummaryTheextant landplantsareuniqueamongthemonophyleticcladeofphotosyn-thetic eukaryotes, which consists of the green algae (chlorophytes), the charophy-ceanalgae(charophytes), numerousgroupsof unicellular algae(prasinophytes)and the embryophytes, by possessing, rstly, a sexual life cycle characterized by analternation between a haploid, gametophytic and a diploid, sporophytic multicellu-largeneration;secondly,theformationofeggcellswithinmulticellularstructurescalled archegonia; and, thirdly, the retention of the zygote and diploid sporophyteembryowithinthearchegonium. Wereviewthedevelopmental, paleobotanicaland molecular evidence indicating that: the embryophytes descended fromacharophyte-like ancestor; this common ancestor had a life cycle with only a haploidmulticellulargeneration;andthemostancient(c.410Myrold)landplants(e.g.Cooksonia, Rhynia and Zosterophyllum) had a dimorphic life cycle (i.e. their hap-loid and diploid generations were morphologically different). On the basis of thesendings, we suggest that the multicellular reproductive structures of extant charo-phytes and embryophytes are developmentally homologous, and that those of theembryophytesevolvedbyvirtueoftheco-optionandre-deploymentofancientalgal homeodomain gene networks.ContentsSummary 27I. Introduction 28II. Developmental constraint or a phyletic legacy? 29III. Green plant phylogeny 29IV. The ancestral green plant life cycle 31V. Haplobiontic or diplobiontic life cycles? 32VI. Pseudo-archegonia, plasmodesmata, and parenchyma 33VII. Genomic re-deployment and embryophyte reproduction 35VIII. Developmental homologies? 35IX. Isomorphic or dimorphic? 36X. Conclusions 38Acknowledgements 39References 39NewPhytologistReview The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741 27www.newphytologist.orgI. IntroductionOneofthemostimportantbiologicaleventsinthehistoryof life was the successful colonization of the terrestrial land-scape bygreen, multicellular plants andtheir subsequentrapiddiversicationduringtheearlyPaleozoic(Chaloner,1970; Graham, 1993, 1996; Niklas, 1997; Raven &Edwards, 2001; Taylor etal., 2009). This key event, whichwasunknowntoDarwin(1859),pavedthewayforterres-trial animalevolution, alteredgeomorphologyby accelerat-ingsoil formationandmodifyinghydrologypatterns, andthusirrevocablychangedtheEarthsclimate(Chaloner&Lawson, 1985; Willis &McElwain, 2002). Authoritiesdiffer regarding when the land plants rst appeared(Fig.1a). Somelines of evidenceindicatethat microfossilassemblagesof sporesfromtheLowerMiddleOrdovicianare the oldest remains of terrestrial plant life, whereas otherspoint toaSilurianEarlyDevonianinvasion(Grayetal.,1974; Gray, 1985; Strotheretal., 1996; Beck&Strother,2001; Wellman etal., 2003), although reports of Neoprote-rozoic terrestrial soil crusts containing photosyntheticorganisms(ofa cyanobacterialnature?)must beconsidered(see Knauth&Kennedy, 2009). What canbe saidwithmorecertaintyis that themodern-daydescendants of therstsuccessful landplantscomprisea monophyletic group,the Embryophyta (KingdomPlantae). The living repre-(a) (b)Fig.1 Reconstruction of an ancient aquaticterrestrial landscape, with the earliest multicellular land plants, adapted from a drawing of Z. Buri-an (c. 1945) (a). Comparison between the diplobiontic and haplobiontic life cycles with some representative botanical examples (embryo-phytes and two aquatic charophytes, Coleochaete and Chara, respectively) (b). In the diplobiontic life cycle, the haploid and diploid phases(gametophyte, G, and sporophyte, S, respectively) are multicellular. In the haplobiontic-haploid life cycle, only the haploid phase is multicellu-lar. The haplobiontic-diploid life cycle (in which the diploid phase exclusively expresses multicellularity, such as in our species and other animals)is not shown. n=number of chromosomes per haploid cell.28 Review Tansley reviewNewPhytologist The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgsentatives of this taxon include the paraphyletic nonvascularplant lineages(colloquiallyreferredtoasthebryophytes)and the tracheophytes (i.e. lycophytes, ferns, horsetails andseed plants).Numerouslinesofevidencesupportthecontentionthattheembryophytesaremonophyleticandcloselyrelatedtothegreenalgae(KingdomsProtistaandProtoctista).How-ever, the embryophytes are unique among all extant lineagesinpossessingthreeimportantandinterrelatedreproductiveattributes. First, they possess a sexual life cycle that requiresanalternationbetweenamulticellularhaploidgeneration,which produces sperm and egg cells (the gametophyte), anda multicellulardiploidgeneration, which produces meiosp-ores withsporopollenin-richwalls (the sporophyte). Sec-ond,they develop multicellular, parenchymatous structuresthat produce eggs and sperm (called archegonia and antheri-dia, respectively). Third, theyretainthefertilizedegg(i.e.the zygote) withinthe archegonium, whereinthe sporo-phyte embryo is nurtured and protected (Walbot& Evans,2003). The retention of the diploid embryo within thearchegoniumis thereasonwhythelandplants arecalledembryophytes and why the older literature referred tothem as the Archegoniatae (Campbell, 1905; Bower, 1908).II. Developmental constraint or a phyleticlegacy?Whetherthearchegoniatediplobionticlifecycle wasessen-tial for (or merely coincidental to) the evolutionary and eco-logicalsuccessoftherstmulticellularlandplantsremainsproblematic. Theretentionof this lifecyclemayreect adevelopmental constraint or a phyletic legacy, that is, a fea-turethateithercouldnotbeorwasnotlostonceacquiredbythelastcommonancestortoallembryophytes.Alterna-tively, this life cycle may have been retained because it con-ferred functional advantages that pregured (or wererequisitefor)survivalandreproductivesuccessinanaerialandpotentiallydesiccatinghabitat (Fig.1a). Adhocadap-tivescenarioscanbeeasilyconstructedtoargueinfavorofthe latter, whereas recent insights from plant developmentalgenomics suggest that very ancient algal gene networks wereco-opted during the evolution of the embryophyte life cycleand multicellular body plan (Niklas & Kutschera, 2009).In the light of this uncertainty, this article has two goals.The rst is to review the available phycological, paleobotan-ical, developmental andmoleculardatathat shedlight onhow the archegoniate diplobiontic life cycle may haveevolved.Thesecondistoexplorehowthesedatainuencethe interpretations of developmental homologies amongembryophyte reproductive structures (i.e. antheridia, arche-goniaandsporangia). Thesegoals dictatethestructureofthis article, whichconformstoaconcept mapdominatedby three axes (Fig.2). The rst of these axes focuses on theenvironmental context inwhichearlylandplantsevolved,grew and reproduced. The environmental context is pivotaltotracingtheevolutionofanylifecycle,becausethemostancient embryophytes requiredaccess toliquidwater forthe successful fertilizationof their eggs. The secondaxisfocusesontheplantbodyplanandthetransition fromtheunicellulartothemulticellularcondition. All theavailableinformationindicatesthattheancestral conditionforeachof the major green plant lineages involved a unicellularbodyplan,andthatmulticellularityisaderivedevolution-ary condition. The thirdaxis deals directly withthe lifecycle concept. For the purposes of our review, only two lifecyclesarerelevant, oneinwhichtwomulticellulargenera-tions occur andanother inwhichonly one multicellulargeneration exists, i.e.thediplobionticand haplobionticlifecycles, respectively (see Fig.1b). Because terminology, suchas diplobiontic and haplobiontic, may be unfamiliar tosome (and used in different ways by others), we provide def-initionsfortheseandothertechnicalwordsandphrasesasused in the context of this article (Table1).III. Green plant phylogenyConcept maps help to establish logical transformationalalternatives among critical character states (e.g. terrestrial vsaquatic, unicellularvsmulticellular; haplobionticvsdiplo-biontic life cycles). However, taken in isolation, they cannotidentifythe polarityof evolutionarytransformations (e.g.aquatictoterrestrialvsterrestrialtoaquatic).Forourpur-pose, a stringent cladistic hypothesis is required, because thephylogenetic relationships amongthe various greenplantlineages are very complex and because a well-supportedcladogramprovidesaframeworkwithwhichtodeducetheFig.2Concept map with three major themes (axes) underlying asequential exposition (steps 16) of the evolution of the land plantlife cycle. H-d, haplobiontic-diploid; H-h, haplobiontic-haploid. Theaquaticterrestrial axis is illustrated in Fig.1a. See text for details.NewPhytologist Tansley review Review 29 The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgevolutionary transitions leading to the embryophyte lifecycle. Inthissection, wereviewthephylogeneticrelation-shipsamongthegreenplantlineagesasapreludetomap-ping life cycle evolutionary transformations. All currentpalaeobotanical, cytological, physiological and moleculardata indicate that the green algae (i.e. the Chlorophyta sensuSmith, 1950) andtheEmbryophytasharealast commonancestor (Mattox&Stewart, 1984; Mishler &Churchill,1985; McCourt, 1995; Karol etal., 2001; Scherpetal.,2001; Lewis &McCourt, 2004; Archibald, 2009), whichwas a unicellular agellate that evolved as a result of ancientendosymbioticeventsinvolvingaprokaryotichostcellanda cyanobacterial-like photoautotroph (Bhattacharya &Medlin, 1995; Kutschera &Niklas, 2004, 2005, 2008)(Fig.3).Numerouslinesofevidencefurthershowthattheembryophytes descended froma last common ancestorshared with the Coleocheatophyceae, Charophyceae andpossiblyother lineages (suchas theZygnemophyceaeandKlebsormidiophyceae), which collectively comprise thegreen algae colloquially called the charophytes (Karoletal., 2001; McCourt etal., 2004). Taken in isolation, theColeocheatophyceaeCharophyceae lineage is relativelysmall in terms of species numbers and includes species withunicellular and multicellular body plans, some of which areadaptedto, oratleastcapableoftolerating, somedesicca-tion (Fig.3).The evidence for the monophyly of the charophyteembryophyte lineage (collectively referred to as the strepto-phytes) is extensive. Inadditiontoproducing cell wallscontaining cellulose, chloroplasts withstackedgrana andchlorophylls a andb, bi- or multiagellatedcells (whenmotilecellsarepresent)andstarchastheirprimaryphoto-synthate,thecharophytesand embryophytesalsoshare fea-tures not found in any other green algae, such as, forexample, several enzyme systems (e.g. glycolate oxidase),motor organelles with asymmetrically inserted agella,Table1 Denitions of key words and phrases used in the context of this articleAntheridium The multicellular, sperm-producing structure of the embryophytes, consisting of a sterile jacketof cells surrounding spermatogenous cellsArchegonium The multicellular, egg-producing structure of the embryophytes, consisting of a neck,neck canal cells and a venter surrounding the eggBody plan The phenotypic architecture that distinguishes one group of organisms from another;the processes that obtain an organisms organized growth and developmentDimorphic The presence of substantive phenotypic differences between the haploid and diploid phases(generations) in the life cycle of an organism; in phycology, heteromorphic(i.e. morphologically different haploid and diploid generations)Diplobiontic A life cycle that involves the alternation of two multicellular phases(one haploid and another diploid) to complete sexual reproduction; also known as thealternations of generations and as the diplohaplontic life cycle, e.g. mosses and fernsGametangia Multicellular gamete-producing structures, e.g. antheridia, archegonia, globules and nuculesGametophyte The multicellular haploid phase in a plant life cycle that produces gametes (sperm or eggs, or both)Globule Sperm-producing multicellular organ of charalean algaeHaplobiontic A life cycle involving only one multicellular generationHaplobiontic-diploid A haplobiontic life cycle in which the only multicellular generation is diploid,e.g. Homo sapiens and other vertebratesHaplobiontic-haploid A haplobiontic life cycle in which the only multicellular generation is haploid;one in which the only diploid phase is the zygote; in phycology, equivalent tohaplontic, e.g. charophycean algaeHomologous One or more traits characterizing two or more phyletically related taxa that emerge asa result of shared highly conserved ancestral structures, genetic networks or mechanism(s)Isomorphic The absence of substantive phenotypic differences between the haploid and diploid phases(generations) in the life cycle of an organismNucule Egg-producing multicellular structure of charalean algaeOogonium In phycology, a cell specialized to function as an eggParenchyma A tissue composed of not distinctly specialized and generally uniformly appearing livingcells with thin primary cell wallsParenchymatous tissue construction A tissue in which cells have the capacity to divide in any plain with respect to the principalbody axis and in which primary or secondary plasmodesmata develop at the majority of cellwalls shared among neighboring cellsPlasmodesmata Microscopic channels traversing the cell walls of embryophytes and some algae that enableintercellular symplastic transport and communicationSporophyte The multicellular diploid phase in a plant life cycle that produces sporesStreptophytes An informal taxonomic term referring to the charophyteembryophyte lineageZygotic meiosis Meiosis occurring after the fertilization of the egg without any intervening mitotic cell divisions.In multicellular algae, zygotic meiosis obtains a haplobiontic-haploid life cycle30 Review Tansley reviewNewPhytologist The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgdissimilar agella roots with a multilayered structure, persis-tent mitotic spindles, open mitosis and phragmoplasts(Mattox & Stewart, 1984; Graham, 1993; McCourt, 1995;Graham&Wilcox,2000;Karol etal.,2001;Scherp etal.,2001; McCourt etal., 2004).Nevertheless, although all green plants are monophyletic,the most recent phylogenies consistently identify a deepgenomic dichotomy betweenthe streptophytes andthreecladistically well-supported lineages (i.e. the Chlorophyceae,Trebouxiophyceae and Ulvophyceae), which are collectivelyreferredtoasthechlorophytes. Likethecharophytes, thechlorophytes are ecologically diverse and include specieswith unicellular and multicellular body plans, some ofwhich can survive in subaerial or emergent habitats (Fig.3).Thedeepstreptophytechlorophytedivide is occupiedby an assortment of lineages represented by unicellularspecies, collectively calledprasinophytes (Fig.3), whosephylogenetic relationships remain problematic (Sym&Pienaar, 1993; Lewis &McCourt, 2004). Althoughtheexistence of six or seven prasinophyte lineages is sup-ported by molecular data (e.g. Zignone etal., 2002),thesealgaearebestviewedasagradeof cellularorganiza-tionemergingfromthebaseof thegreenplant clade. Assuch, theyhavethepotential toshedlightonthefeaturescharacterizing the last commonagellate ancestor totheentiregreenplanttreeoflife.IV. The ancestral green plant life cycleThe precise phylogenetic relationships amongthe prasin-ophytes, chlorophytes andstreptophytes will undoubtedlybe modied as more taxa are examined and more dataare incorporated into cladistic analyses. However, givencurrent information, threeconclusions canbedrawn: thegreen plants are monophyletic; the phyletic dichotomyseparatingthe chlorophytes andthe streptophytes is occ-upied by prasinophytes; and the streptophytes des-cended from a unicellular freshwater alga. Here, wereviewdata that support twoadditional conclusions: theancestral lifecycleinall of themajor greenalgal lineagesinvolvedzygotic meiosis andwas thus haplobiontic (Fig.1b); and the derived green plant diplobiontic life cycleevolved at least twice, once among the chlorophytes(Ulvophyceae)andagainamongthestreptophytes(charo-phytes andembryophytes).These assertions are based on two lines of evidence. First,amongextantunicellularandmulticellulargreenalgae(i.e.prasinophytes, chlorophytes and charophytes) for whichsexual reproductionhas been documented, most have a lifecycleinwhichtheonlydiploidcell is thezygote(Smith,1950; Bold&Wynne, 1978; Graham&Wilcox, 2000;Lee, 2008). Second, although sexual reproduction has beendocumentedforveryfewspeciesinthebasal prasinophytelineages,thosethathavebeencorroboratedinvolvezygoticmeiosis (e.g. Nephroselmis olivacea; Suda etal., 1989)(Fig.4a).Thus,forthemajorityofgreenalgae,theadultormatureorganisminthesexuallifecycleishaploidandfunctionsreproductivelyasthegametophytegenerationinthe embryophyte life cycle (Graham & Wilcox, 2000; Nik-las & Kutschera, 2009).As noted, plant life cyclesinvolvingonlyone multicellu-lar individual are called haplobiontic (in contrast withFig.3Phylogenetic relationships among themajor green plant lineages based on an anal-ysis of DNA sequence data. Dichotomousbranches shown as broken lines indicateweakly supported portions of the tree. Thephyletic position of the Mesostigmato-phyceae is particularly problematic (denotedby ?). The distributions of different habitatpreferences, body plans and life cycles areindicated by symbols (see lower box).Adapted from Lewis & McCourt (2004).NewPhytologist Tansley review Review 31 The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgdiplobionticlifecycles withtwomulticellular individuals;Fig.1b). Two variants of the haplobiontic life cycle are pos-sible. Oneinwhichthemulticellulargenerationisdiploid(the haplobiontic-diploid life cycle; Hd) and one in whichthe haploid generation is exclusively multicellular (haplobi-ontic-haploid; Hd) (see Fig.2, node 4). Therefore, lifecyclesinvolvingzygoticmeiosisareclassiedashaplobion-tic-haploid(Table1). Clearly, nomulticellular generationexistsinthecaseofunicellularalgae.Thesexuallymatureindividual functions either indirectly or directly (i.e. with orwithout intervening mitotic cell divisions) as the adultorganismandasagamete.Therefore,thehaplobionticvsdiplobionticterminologyislargelyirrelevant.Nevertheless,the life cycles of unicellular algae, such as Nephroselmis oliv-acea, andmulticellularalgae, suchasMonostromagrevillei,arefundamentallythesame(Fig.4a,b, respectively). Bothare dened by zygotic meiosis. The only fundamentaldistinctionthat conceptuallyseparates the twolife cyclesiswhether(andwhere)multicellularityisdevelopmentallyexpressed.Incontrast withthebroadphyletic distributionof ha-plobiontic-haploidlifecycles,diplobionticlifecyclesoccurinonlyonegreenalgallineagetheUlvophyceae(Fig.3).Three of the six orders withinthis class are reportedtocontainspecieswithdiplobionticlifecycles(i.e. theClad-opherales, Trentepohliales and Ulvales; see Graham&Wilcox, 2000; Lewis &McCourt, 2004; Lee, 2008andreferencestherein). Amongthesespecies, somediplobion-tic life cycles are isomorphic (e.g. Ulva), whereas othersare dimorphic (e.g. Derbesia). However, evenamongthevariousUlvophyceae, thediplobionticlifecycleappearstobeanevolutionarilyderivedcondition, becausemoleculardata suggest that the Ulotrichales are basal in the Ulvophy-ceae(OKelly etal.,2004),andbecauseulotrichaleanalgaehave haplobiontic-haploid life cycles, e.g. Ulothrix andMonostroma(Fig.4b). Thehaplobiontic-haploidlifecycleis also well representedamong the acellular (siphonous)ulvophyceanmarinealgae.Theselinesofevidenceindicatethat the diplobiontic life cycles of the Embryophyta andUlvophyceae are the result of convergent evolution (seeFig.3).V. Haplobiontic or diplobiontic life cycles?Was thelast commonancestor totheCharophyceae andEmbryophytaunicellularormulticellular?Thisquestionisimportant becauseits answer provides aninsight intotheevolutionof theembryophytelifecycle. Consider that, ifthelastcommon ancestor wereunicellular,thecapacityformulticellularitycouldhaveevolvedineitherthehaploidordiploidgeneration, orbothsimultaneously(Fig.5a,b)apossibility that opens the door tomany conceivable lifecycle variants as the ancestral condition. Alternatively, if thelast common ancestor were multicellular and had a life cycleinvolving delayed zygotic meiosis, the diploid generation inthe embryophyte life cycle (i.e. the sporophyte) would be anevolutionary innovation.The phyletic distribution of unicellular species at the baseofthestreptophytelineagehighlightstheproblematicnat-ureoftheanswertothisquestion,asillustratedbythecla-distic position of the monotypic Mesostigmatophyceae(Fig.3). Mesostigma vividaisanasymmetricalcellthatwasoriginally classied as a charophyte on the basis of its agel-lar ultrastructure (Melkonian, 1989). Subsequent molecularanalyses of 18SrRNAsequences indicatedthat thegenuswas closelyrelatedtoChaetosphaeridum, whichledtotheestablishment of a newclass, the Mesostigmatophyceae(Marin &Melkonian, 1999). However, Delwiche etal.(2002) demonstrated that Chaetosphaeridum is a charophyteand, on the basis of rbcl sequences, concluded that Mesostig-ma isa sister taxon tothestreptophytes. Subsequently, Yo-shii etal. (2003) argued that Mesostigma represents an early(a)(b)Fig.4Diagrammatic comparison of the life cycles of the prasino-phyte Nephroselmis olivacea (adapted from Suda etal., 1989) (a)and the ulotrichean alga Monostroma grevillei (adapted fromGraham & Wilcox, 2000) (b).32 Review Tansley reviewNewPhytologist The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgevolutionarylineageandplacedtheMesostigmatophyceaeamong the prasinophytes (Fig.3).The phylogenetic position of Mesostigma remains conten-tious(seeLewis&McCourt,2004).However,itsphyleticposition at the base of the chlorophytestreptophytedivide, in tandem with the antiquity of lineages containingnumerous semi-aquatic and terrestrial unicellular species(i.e. Chlorokybophyceae, Klebsormidiophyceae and Zy-nemophyceae), suggests that a variety of life cycles may haveevolved(anddisappeared) over theearlycourseof charo-phyceanevolution(seeFig.3).Indeed, oneintriguinglineof speculation is the prospect that important life cycle evolu-tionary innovations occurred among unicellular or lamen-touscharophytesservingasphycobiontsinancientlichen-likeorganisms.Currently,nolichenisknowntocontainacharophyceanphycobiont (Friedl &Bhattacharya, 2006).However, it is possible that the ancient co-evolutionary his-toryofthelandplantsandmycorrhizawaspreguredbyamutually benecial relationship between ancient charo-phytesandfungithatcanbebroadlythoughtofaslichen-like symbiotic organisms (McCourt etal., 2004).Althoughthenatureof themostancientlandplantlifecycle cannot be assertedcurrently, the available evidenceindicatesthattheancestortothestreptophyteswasmulti-cellular and possessed a haplobiontic-haploid life cyclesimilar to that of Coleochaete and Chara. If this suppositionistrue,thelandplantsporophytegenerationwasanevolu-tionaryinnovationresultingfromdelayedzygoticmeiosisandtheintercalationofoneormoremitoticcellulardivi-sions. Put differently, the rst embryophyte sporophyte wasa multicellular zygote. Whether this life cycle rst appearedinanaquatic, semi-aerial oraerial environment is conjec-tural. Althoughthetransitionfromahaplobiontic-haploidtoadiplobionticlifecyclemayhavecomeat acost withregard to the growth of the haploid generation (as indicatedbystudiesonmosses; seeEhrlenetal., 2000; Rydgren&kland,2002),thediplobionticlifecycleconfersadaptivebenets across a broad range of habitats and environmentalconditions (e.g. the numerical amplication of zoospores ormeiosporesresultingfrompossiblyrarefertilizationevents,andthe possibilitytooccupytwodifferent niches inthesamegeneralenvironment),asattestedbythereproductiveandecological success of ulvophyceanalgae andembryo-phytes with free-living gametophytes.Nevertheless, if theevolutionarytransformationfromahaplobiontic-haploid to a diplobiontic life cycle occurred inafreshwater or terrestrial habitat, whichis almost acer-tainty, therst sporophytes wouldhardlyqualifyas landplants, as they would have grown on maternal gametophytesattached, in turn, to a hydrated substrate, and thus are moreproperly thought of as air plants (see Fig.1a).VI. Pseudo-archegonia, plasmodesmata andparenchymaWhether the rst charophycean algae to evolve a diplobion-ticlifecyclewerearchegoniatesisanotherchallengingandunresolvedquestion. Thefossil recordof theearliest landplants is especially sparse and problematic, and there isnothing in the diplobiontic life cycle concept that stipulatesthe manner in which sperm or eggs are produced (Wellmanetal.,2003).Inaddition,asnotedearlier,thediplobionticlifecycleis not uniquetotheembryophytes (seeFig.3).However,itisverylikelythatthelastcommonancestortothe streptophytes had reproductive structures that func-tionedinsome, ifnotmany, waysliketheantheridiaandarchegonia of embryophytes, such as Equisetum (Lycopodia-cae), a seedless land plant (Fig.6a,b).This assertion rests on three observations. The zygotes ofmany, albeit not all, species in the Coleochaetophyceae andall species in the Charophyceae are retained by the gameto-phyte, during which many species nourish and protect themfor short, albeit developmentally substantive, periods oftime; and the most evolutionarily derived charophyceanspecies, suchas stonewortsof the genus Chara, have multi-cellular and morphologically complex gametangia (Fig.6c,d). In the case of Coleochaete (see Fig.1b), sterilelamentsdeveloparoundtheoogoniumafterfertilization.(b)(a)Fig.5Diagrammatic rendering of the hypothetical transformationof an ancient prasinophyte life cycle (a) (depicted as that of Nephro-selmis olivacea; see Fig. 4a) into a diplobiontic life cycle (b). Delayedzygotic meiosis and the intercalation of mitotic divisions results in amulticellular sporophyte and mitotic divisions of meiospores beforeplasmogamy results in a multicellular gametophyte.NewPhytologist Tansley review Review 33 The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgInthe case of charaleanspecies, sterile cells enveloptheoogonium before fertilization. Indeed, the sperm-producingorganofChara(theglobule)isfunctionally(anddevelop-mentally) similar in many ways to the antheridium, whereasthe egg-producing structure (the nucule) canbe calledapseudo-archegonium on the basis of its capacity to protectand provide the egg and zygote with nourishment for a notinconsiderable time (Fig.6c,d).Anotherphysiologicallyimportantfeaturesharedbythecharophytes and embryophytes is the capacity to form plas-modesmata(Graham, 1982), whichhas evolvedindepen-dently many times in different algal lineages and inde-pendently within the Chlorophyceae and again in theCharophyceae (Raven, 1997). Among the streptophytes, theability to form these symplastic connections among adjoin-ing cells is restricted to the Coleochaetophyceae (specicallyColeochaete, see Fig.1b), Charophyceae(Fig.6c,d) and theEmbryophyta (Brown etal., 1994; Cook etal., 1998). Theability to form plasmodesmata permits active polar transportof large molecular weight solutes across adjoining cell walls,whichfacilitates thetargetingandnutritionof specializedcells (see Jansen, 2001; Lucas etal., 2001). It can also play apivotal roleinthephysiological control ofembryogenesis.More detailed studies are required to determine whether cha-rophycean plasmodesmata are typically primary or secondaryinnature. Theformerdevelopduringcytokinesisandcellwall deposition; the latter develop after cytokinesis and mayappearaftersecondary wall deposition. Whether primaryor secondary plasmodesmata formduring or after histo-genesis is important, because it helps toresolve whetherthetissuesinwhichplasmodesmatadeveloparetrulypar-enchymatous, andbecauseprimaryand(complex)second-aryplasmodesmatahavedifferent protein-trafckingfunc-tions, whichcaninuenceorganogenesis (e.g. Itayaetal.,1998). Regardless of these subtleties, primary plasmo-desmatahavebeendemonstratedforatleastonespeciesofChara (Brown etal., 1994; Cook etal., 1998), andultrastructural studies suggest that the nodal regions ofChara have a parenchymatous tissue structure (Pickett-Heaps, 1975; Cook etal., 1998).(a) (b)(c) (d)Fig.6Comparisons among the antheridiumand archegonium of the vascular land plantEquisetum (a and b, respectively) and thereproductive organs (nucule and globule,with gamete-producing tissues) of the Chara-lean alga Chara (c and d, respectively). c,coronal cells; e, egg; g, globule; n, neck cells;nu, nucule; o, oogonium sc, spermatogenouscells; sj, sterile jacket cells; spc, sperm cells; v,venter.34 Review Tansley reviewNewPhytologist The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgVII. Genomic re-deployment and embryophytereproductionTheabilitytoformplasmodesmataandparenchymaisnotarequisitefor theformationof morphologicallycomplexmulticellular structures, suchas the gametangia of Chara(Fig.6c,d). The nucule andglobule of Chara andothercharalean algae arecomposed of branched laments, whichonly give the appearance of having a parenchymatous tissueconstruction. However, the ability to form parenchyma andplasmodesmata is animportant attribute of the embryo-phytes, becauseit establishes complexandphysiologicallyintegrated symplastic interconnections via primary and sec-ondary plasmodesmata formation that are required for spo-rophyte embryogenesis and development.Indeed, recentstudiesofhomeodomain-containingtran-scriptionfactor genes suggest that anintriguinggenomicredeployment strategy has attendedthe evolutionof thearchegoniate diplobiontic life cycle. For example, amongthebestknownofthesegenesis theMADS-boxgenefam-ily, whichhas beenextensively studied inthe oweringmodel organismArabidopsis thaliana. This genefamilyisdividedintotwosubfamilies,referredtoastypeIandtypeII.Thereare45typeIIgenes,whichare alsoreferredtoasMIKC factors (for MADS DNA-binding domain, interven-ingdomain,keratin-likedomainandC-terminaldomain);thetypeIIgroupcanbefurthersubdividedintoMIKCCand MIKC* geneson the basis of theinferredevolutionaryhistory of the family. MIKC* proteins tend to have longer Idomains and less-conserved K domains than do the MIKCCproteins. SequencesencodingMIKCCandMIKC*factorshavebeen identiedinbryophytesandlycopods,aswellasingymnospermsandangiosperms, whichsuggeststhattheMIKC*andMIKCCgeneshaveevolvedindependentlyforat least 450Myr. Theexpressionof MIKC-typegenes inangiosperms occurs only after the specication of thevegetative to inorescence meristemtransition, which ismediated by the transcription factor encoded by FLORICA-ULA LEAFY (FLO LFY). In ferns, FLO LFY homologs areexpressed predominantly in sporogenous meristematictissues, but MADS-box gene expression is not closely corre-lated, suggesting that these genes have not yet been subordi-natedtoFLO LFYregulation. InthemossPhyscomitrella,two FLO LFY paralogs (PpLFY-1 and PpLFY-2) arerequired for the rst division of the zygote and early sporo-phyte embryogenesis (Henschel etal., 2002; Tanahashietal., 2005), whereas MADS-boxgene expressionoccursduringCharaglobularis gametangiumdifferentiationanddeclines after fertilization (Tanabe etal., 2005).It is therefore reasonable to suggest that MADS-boxgenes originally functioned in the differentiation of haploidreproductivestructures(e.g. thenuculeandmossarchego-nium) and were subsequently redeployed to function in theformationof sporophyte reproductive structures (e.g. thefern sporangium). Such combinatorial homeodomain-basedtranscriptional control of reproduction may have extremelydeepphylogeneticroots.Ectopicexpressionofthehomeo-proteinsGsp1andGsm1intheplusandminusstrainsoftheunicellularchlorophyteChlamydomonas activatesvege-tative haploid cells to form zygote-like structures (Lee etal.,2008). Likewise, Gsp1 and Gsp2 are members of the TALE(threeaminoacidloopextension)homeodomain-contain-ingtranscriptionfactors,whichincludetheclass1KNOXand class 2 KNOX proteins. Homeodomain gene networks,similartothoseinlandplants,havebeenreportedforpra-sinophytes (e.g. Micromonas), which are postulated to revealthe attributes of the last common ancestor of all greenplants (Worden etal., 2009) (see Fig.3).VIII. Developmental homologies?Therecruitmentandredeploymentofhomeodomaingenenetworks underlying much of the evolution of strepto-phyte reproduction may help to explain why charaleangametangia andembryophyte antheridia, archegonia andsporangiasharethesamefundamental developmentalcho-reography(Fig.7).Perhaps the most obvious shared attribute of these multi-cellular structures is that each develops from a single super-cial meristematicinitial. Inthecaseof charaleanglobuleandnucule,thisinitialisanodalcell(Fig.7a);inthecaseofembryophytes,itistypicallyanepidermalcell(Fig.7b).Charalean antheridium induction involves an unequal divi-sion of the nodal initial cell. The smaller of the two deriva-tives develops into a stalk; the larger, apical cell undergoes aseriesofcellulardivisionsthateventuallyproduceexternalshieldcells that surroundstalks andbranchedstructures(manubria) fromwhichspermlaments radiate (Pickett-Heaps, 1975). The development of the charaleannuculealso begins from a single nodal cell that undergoes unequalcell divisions toformabasal stalkandthetubecellsthatgyrate around a centrally located oogonium (Pickett-Heaps,1975). In much the same way, sporangial inductioninvolvespericlinaldivisionofoneormoreepidermalcells.Among eusporangiate species, the innermost derivativesgive rise to sporogenous cells, whereas the outermostdevelopintothesporangiumwall (Fig.7b). Embryophytegametangia(antheridiaandarchegonia) development alsobeginswhenasingleepidermal cell undergoesapericlinaldivision. The innermost cells resultingfromthis divisiondevelopintospermatogenous cells, or theneckcanal andegg cells (for details, see Campbell, 1905; Bower, 1908;Gifford & Foster, 1989).Numerous differences exist inthe development of eu-andleptosporangiaandinthedevelopment of antheridiaandarchegonia. Forexample, thesporogenouscell initialsin the eusporangium develop from the innermost periclinalderivativesofthesupercialsporangialinitials,whereastheNewPhytologist Tansley review Review 35 The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgsporogenouscellsoftheleptosporangiumtracetheirdevel-opmental origins toouter periclinal derivativecells. Like-wise, charalean and embryophyte development differ inmany ways. For example, the charalean oogonium occupiesanapical (albeitenveloped)position, whereastheembryo-phyte egg cell develops froma hypodermal derivative.Likewise, thenuculeandglobulehaveapseudo-parench-ymatous (lamentous) tissue construction, whereas sporan-gia, antheridia and archegonia are parenchymatous (Gifford& Foster, 1989; Graham & Wilcox, 2000).Nevertheless, wesuggestthatthereissufcientdevelop-mental and molecular evidence to conclude that theembryophytesporangiumis homologous totheantherid-ium archegoniumas a result of homeodomaingene net-work recruitment fromthe gametophyte generation andredeployment in the sporophyte generation. In this context,we use the concept of homology sensu Shubin etal. (1997),namely a correspondence in growth and differentiationresulting from highly conserved and deeply ancestral geneticmechanisms. Likewise, webelievethatarchegoniaandan-theridia are developmentally homologous to charalean gam-etangia, i.e. embryophyte gametangia are homologous tothenuculeandglobule(Fig.7).Thisperspectiveisconsis-tentwith current knowledge ofthemolecular developmen-tal biology of streptophyte reproductive structures. It is alsoconsistent withthe evolutionof the embryophyte diplo-biontic life cycle from the haplobiontic-haploid life cycle ofa charalean common ancestor. The alternative assertion thatembryophytesporangiaarehomologoustoleavesisfarlesstenable (Kenrick & Crane, 1997a,b).IX. Isomorphic or dimorphic?We have arguedthat the ancient aquatic ancestor toallgreeneukaryotes (Kingdoms Protoctista and Plantae) was asingle-celledagellate(Fig.3) withalifecyclethat alter-natedbetweenahaploidgenerationthatfunctionedastheadult+gameteandamoreorlessephemeral single-celledzygote(Fig.1b). Thetraditional botanical viewprecludesassigning such an organism a diplobiontic or a haplobionticlife cycle, because multicellularity is not expressed in this lifecycle. Nevertheless, this kindof organismhasanalterna-tionof generations, albeit unicellular ones. Accordingly,anyconsiderationof thelifecycleof theearliest Urform(prototype) of all landplants necessarilybegins byaskingwhether the immediate ancestor tothe streptophytes wasunicellular in both phases of its life cycle (as was its aquaticprecursor), orwhetheroneorbothof itslifecyclephaseswas multicellular. This consideration is cast in botanical tra-dition by asking whether the life cycle was isomorphic (bothlife forms are the same) or dimorphic (twodifferent lifeforms) (see Fig.2, node 5; Table1).(b)(a)Fig.7Comparisons among the developmentof charalean gametangia (a) and the repro-ductive structures of embryophytes (b). Thecharalean globule and nucule each developfrom a single supercial nodal cell initial (a).The embryophyte eusporangium, antherid-ium and archegonium typically develop froman epidermal cell initial (b). Tissues directlyinvolved with reproduction (e.g. sperm, eggand sporogenous cells) are shaded.36 Review Tansley reviewNewPhytologist The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgThereareobvious advantages tomulticellularityfor anorganismlivinginasubaerialenvironment,e.g.protectionagainst UV exposure and dehydration (Niklas, 1997;Raven, 1999, 2002). However, the most ancient green landplants may have inhabited the soil or evolved from a lichen-likeorganism,andthusmayhavebeenprotectedbymois-ture-ladenboundarylayers (Stebbins &Hill, 1980; Readetal., 2000). Whatisclearisthat, overmanygenerations,the landplants became multicellular, andwe necessarilyneedtoknowwhether this innovationoccurredsimulta-neouslyinboththegametophyteandsporophytegenera-tion, or whether one generationacquiredmulticellularitywhilst the other generation subsequently acquired this bodyplan.Onthe basis of the distributionof life cycles amongextant greenplants (Fig.3), it is logical toarguethat theseries of life phase transformations achieving multicellulari-ty beganwiththe gametophyte generation, andthat thezygotesoftheancestorsoftherstgreenlandplantswerepreprimedformeiosis. If true, thevegetativephaseof thegametophyte generation is the primal (ancestral) and arche-typical homeforlandplantgeneexpressionandgenenet-work interactions, as well as the effects of heritablemutationsonmorphogenesis. Nevertheless, thealternativepossibilitythatmulticellularityaroserstinthediploid,sporophyticphasecannotbeexcluded, especiallyfromageneticperspective,asasinglemitoticdivisionbeforemei-otic cell division generates eight (not four) potentiallyrecombinantgenotypesfromeachzygote(withconsequentselective advantages), incontrast witha mitotic divisionafter meiosis, which generates two (not one) spore recombi-nant genotypes (withconsequent effects onthestochasticloss of a desirable combination of genes).Another conceptuallyimportant, but as yet unresolved,questionis whether the most ancient embryophytes pos-sessed an isomorphic or a dimorphic life cycle (Fig.2,nodes5and 6). Kenrick&Crane(1997a,b) andSteemansetal. (2009) have argued that the isomorphic alternation ofgenerations is the most ancient, inpart basedonthree-dimensionallypreservedgametophytes inthec. 410Myrold Rhynie Chert (see Kerp etal., 2004; Taylor etal.,2005; Niklas & Kutschera, 2009). As discussed in the previ-ous section, the gametophytes and sporophytes of the mostancientembryophytesundoubtedlysharedsimilargenomicanddevelopmentalrepertories,justastheysharedgenomicsimilarities with their charalean common ancestor. Thus, inthe absence of phenomenologies, such as gene silencing, sexchromosomes or epigenetic effects, differences in ploidymay not have equatedtosignicant gametophytesporo-phyte morphological differences. This perspective isstrengthenedinthelightofsomemodern-daymossesandferns, which can generate sporophyte morphologies directlyfromtheirgametophyticcells(apogamy)andgametophytemorphologies directly fromtheir sporophyte cells (apo-spory).Apogamyandaposporyshowthatthehaploidanddiploid genomes contain much of the information requiredto construct both the gametophyte and the sporophyte bodyplans (Niklas & Kutschera, 2009).Afocusonapogamyratherthanaposporyisjustiedinthe context of our review, because the thesis developed thusfar is that the sporophyte generationevolvedduring thetransitionfroma charalean-like haplobiontic-haploidlifecycle to anembryophyte diplobiontic life cycle. Amongextant species, apogamy can be induced by cell trauma, lowlight intensities, suitable concentrations of sugar or auxin. Itcan also be induced by the deletion of the CURLY LEAF or-tholog inthe moss Physcomitrella(PpCLF). Okanoetal.(2009) havereportedthat gametophyticcells that usuallyform protonema or gametophore apical cells generate meri-stematic apical cells that formbranched morphologies,whichcanbeinducedtoformsporangium-likestructureswiththe exogenous applicationof PpCLF. The resultingmorphologies have been reported to be similar to veryancienttracheophytes, suchasZosterophyllumorCooksonia(Figs8 and 9).ThesendingssuggestthatPpCLFregulatorygenenet-works mayhaveparticipatedintheearlyevolutionof theembryophytesporophyte(Okanoetal., 2009). Spontane-ousmutationoftheCURLYLEAForthologattendingfer-tilization and zygote formation among ancient strepto-phytes may have participatedindelayedzygotic meiosis,and thus the formation of a multicellular diploid phase. It isneverthelessdoubtful thatthemutationofanysinglegenewas sufcient for this important evolutionary transition.Likewise, it is uncertain whether the sporophyte generationevolved as a consequence of delayed zygotic meiosis orprecocious zygotic mitosis. Molecular analyses of angiospermmega- and microsporogenesis and mega- and microgameto-genesisindicatethatnumerouscomplexgenenetworksareinvolvedinthe initiationor suppressionof meiosis. Forexample, the male sterile multiple archesporial cell (mac1)mutant in maize (Zea mays), which leads to the productionof extra diploid sporocytes in ovules and anthers, appears tocontributetotherestrictionoftheidentityofcellscompe-tent for meioticdivision (see Sheridan etal., 1996; Walbot&Evans,2003),whereasthe MeiosisArrestedat Leptotene1(MEL1) gene inrice (Oryza sativa) is requiredfor spo-rocyctemeiosis(Nonomuraetal., 2007). Moredatafromtaxadeeperwithinthestreptophytelineagearerequiredtoshed meaningful light on the gene networks that participatein early sporophyte embryogenesis.Returningtotheantiquityoftheisomorphicvsdiplobi-onticlifecycle,anumberoflinesofevidenceindicatethatthemostancient embryophytelifecyclesweredimorphic.First, extant monoploid embryophytes do not developapogamous sporophytes, suggestingthat gene duplicationandsubsequent functional divergencepresagedtheevolu-tionofmulticellularsporophytes, whichisconsistentwithNewPhytologist Tansley review Review 37 The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgtheextensiveanalysis of thePhyscomitrellapatens genome(Rensingetal., 2008). Second, embryophyte sporophytesand gametophytes normally develop in very different physi-ological andmechanicalenvironments.Youngsporophytesdevelop within archegonia; free-living embryophyte ga-metophytes develop fromdispersed meiospores. Third,numerous environmental factors inuence early morpho-genesisthatfostersdimorphism(Sinnott,1960).Fourth,ifthemostancientsporophyteswereanintercalated multi-cellulargeneration,itisdifculttoimaginethattheyweremorphologically elaborate indeed, they may have beennothingmorethanthefunctional equivalent of asporan-gium(Niklas,1997).Fifth,thedifferentfunctionalobliga-tions of the gametophyte and sporophyte generations wouldhave sustained and even amplied their ancestral di-morphism. Sixth, the purported life cycles of RhynieChert plants (datedto410Myr), suchasRhynia, arenotisomorphic(Kerpetal., 2004; Tayloretal., 2005; Niklas&Kutschera, 2009). Seventh, there is some evidence(albeit, at this point, veryproblematic) that moreancienttracheophytes, such as Zosterophyllum and Cooksonia(Figs.8,9), may have had dimorphic life cycles (Probst,1986; Niklas & Banks, 1990; Remy etal., 1993; Gerrienneetal., 2006).X. ConclusionsManydetails regardingthe phylogenyof the greenplantlineages (chlorophytes and streptophytes) remain unre-solvedandwill require more data frommore taxa, part-(a)(b)Fig.8(a) Upper part of a mature sporophyte(sporangium, indicated by an arrowhead) ofZosterophyllum rhenanum, an Early Devo-nian (c. 410Myr old) vascular land plant. Afossilized spore is shown in the inset. (b)Reconstruction of the phenotype of a clusterof plants (adapted from Edwards, 1969; andProbst, 1986).(a) (b)Fig.9Purported sporophyte (sporangia indi-cated by arrowheads) attached to its game-tophyte (see arrow and shaded region ininset) of Cooksonia paranensis, an EarlyDevonian (c. 415Myr old) vascular landplant (a) and reconstruction of the pheno-type (b). No vascular tissues or spores wererecovered from this fossil. Although sporeshave been isolated from similar structures onother fossils assigned to the same species, itremains possible that the entire fossil is agametophyte (adapted from Gerrienne etal.,2006).38 Review Tansley reviewNewPhytologist The Authors (2009)Journal compilation New Phytologist (2009)New Phytologist (2010) 185: 2741www.newphytologist.orgicularlyfromthoseresidingatthebaseofthisecologicallyrich clade. The broad phylogeny of the green plants isnevertheless sufcientlywell resolvedtopermit a reason-ably stringent phyletic scaffolduponwhichto trace thecharacter transformations attending the evolution of theembryophytediplobionticlifecycle. Usingthis approach,twoconclusions emerge that will probablystandthe testof future scrutiny. First, the ancestral organismfor theentiregreenplantclade(andforthelineageleadingtothecharophytes) was a agellatedeukaryotic photoautotroph(Fig.3), and, second, theancestral organismtothestrep-tophytes(Coleochaetophyceae,Charophyceae,andEmbry-ophyta) was amulticellular algathat hadahaplobiontic-haploidlifecycleandmorphologicallycomplexgametan-giareminiscentofthoseof Chara(Fig.6c,d).Withfarlesscertainty, we surmise that the earliest land plants(Figs1a,8,9) had a dimorphic diplobiontic life cycle inwhichthehaploid(gametophytic) phasedominated. Sub-sequent evolutionary divergence ledto landplant formsthatretainedthisancestralcondition(representedtodaybythe extant bryophytes) andlineages inwhichthe diploidgeneration became dominant (represented by all extant tra-cheophytes, notably the seed plants, Fig.1b). Althoughspeculative, we further suggest that there is sufcientobservational and molecular data to indicate that thereproductiveorgans of embryophytes (i.e. archegonia, an-theridia, and eusporangia) are homologous structures(sensuShubinetal., 1997) that, inturnarehomologouswiththe multicellular gametangia of the charaleanalgae(the nucule and globule) (Fig.7). These homologiesappearto bethe result of the co-option and re-deploymentof ancient algalgenenetworks.Much speculation surrounds the properties of genes,genenetworks, andevenentireorganisms that favor piv-otal evolutionary transformations that nevertheless con-serve structural and genomic homologies. Although theevidenceissparse, speculationfavorstheeffects of regula-torygenes,ingeneral,and transcriptionfactors, inparticu-lar, as the most probable drivers of evolutionaryinnovation(seeDoebley&Lukens, 1998; Cronk, 2001).However, thefewdetailedstudies of plant developmentalgeneinteractionsareinsufcienttojustifythisviewtotheexclusion of other potentially equally important mecha-nisms,aswitnessedbytherecentndingthatthedevelop-mentalpatterningofthehighlyreducedangiospermmega-gametophytedepends onanasymmetric, location-specicgradient of auxinsynthesis (Pagnussat etal., 2009). Forthis reason, we conclude that future enquiries into thedevelopmental mechanism(s) by which the embryophytelifecycleevolvedwouldprot fromdetaileddiagnoses ofthe molecular drivers of the plant cell cycle, the inductionofmeioticversusmitoticcell division, andahostofotherfundamental phenomena. Scrutinyof meioticgenecandi-dates and factors that contribute to homologous chro-mosome pairingwill be a particularlyimportantand fertileeld of inquiry (seeAble etal., 2009).AcknowledgementsWe thank Dr. P. Gerienne for providing Fig.9a and Dr. J.Raven (the University of Dundee, UK) for many useful sug-gestions. We also thank the College of Agriculture and LifeSciences (Cornell University, Ithaca, USA) and the Alexan-der-von Humboldt-Foundation (AvH, Bonn, Germany) fornancialsupport(AvH-fellowship2009,Stanford Califor-nia, USA to U. Kutschera).ReferencesAble JA, Crismani W, Boden SA. 2009. Understanding meiosis and theimplications for crop improvement. Functional Plant Biology 36: 575588.Archibald JM. 2009. Green evolution, green revolution. Science 324: 191192.Beck JH, Strother PK. 2001. Silurian spores and cryptospores from theArisaig group, Nova Scotia, Canada. Palynology 25: 127177.Bhattacharya D, Medlin L. 1995. 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